Vol. 465: 299–304, 2012 MARINE ECOLOGY PROGRESS SERIES Published September 28 doi: 10.3354/meps09902 Mar Ecol Prog Ser

OPENPEN ACCESSCCESS AS WE SEE IT

Fish ingredients in online recipes do not promote the sustainable use of vulnerable taxa

Charis Apostolidis*, Konstantinos I. Stergiou

Laboratory of Ichthyology, School of Biology, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece

ABSTRACT: Consumer preferences can be influenced by cultural factors, such as recipes. Thus, popular recipes using seafood ingredients could encourage demand for the featured marine spe- cies. We recorded the fish taxa appearing in all online Greek recipes and related the number of recipes in which a taxon is a suggested ingredient to the taxon’s landings and vulnerability to fish- ing. For marine fish, the number of recipes per taxon (henceforth called recipe prevalence) increased significantly with the taxon’s landings. When the effect of landings was removed, recipe prevalence increased significantly with vulnerability to fishing, indicating that more vulnerable taxa appear more frequently in recipes. This pattern should be reversed by eliminating the recipe abundance of taxa that are very vulnerable to fishing and counterbalance such a reduction with an increase in the representation of taxa of low vulnerability, landed in large quantities and cur- rently underrepresented in recipes. Managing recipe composition by educating a small group of stakeholders (i.e. chefs and recipe authors) may be a cost-effective way of promoting fisheries sustainability when compared to directly educating consumers.

KEY WORDS: Consumer influence · Conservation · Landings · Recipes · Vulnerability to fishing

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INTRODUCTION management and aim to influence consumer pre - ferences towards sustainability (Halweil 2006, Most fisheries are depleted and/or are being con- Jacquet & Pauly 2007, Roheim 2009). However, the tinually overfished (Garcia & Rosenberg 2010). Irre- effect of cultural factors, such as recipes, on consumer spective of the magnitude of fisheries mismanage- choices regarding fish consumption has been largely ment (Myers & Worm 2003, Pauly et al. 2003, Hilborn ignored (Levin & Dufault 2010). 2007, Worm et al. 2009), excessive fishing impairs Nowadays, chefs have started taking an energetic ecosystem health (e.g. Jennings & Kaiser 1998, Pauly role in the conservation of fish stocks by recommend- et al. 1998, Stergiou 2002) and has important socio- ing the consumption of sustainably exploited fish, economic implications (e.g. Failler & Pan 2007, Srini- with positive results in most cases. For example, after vasan et al. 2012). Thus, there is a growing concern the launch of the BBC Channel 4 show ‘Fish season’, for the future of fisheries, which, among other actions, fish demand considerably increased, especially for has resulted in the launch of various consumer and that were proposed to replace the overfished market-based actions, such as public information Atlantic morhua (e.g. demand for campaigns and sustainability certification schemes was reported to increase by 167%) (Halweil 2006, Jacquet & Pauly 2007, Roheim 2009). (Tyler 2011). However, such actions have not yet These campaigns complement traditional fisheries been broadly applied to recipe websites. The impor-

*Email: [email protected] © Inter-Research 2012 · www.int-res.com 300 Mar Ecol Prog Ser 465: 299–304, 2012

tance of online recipes in influencing the public can expert system (see Cheung et al. 2005 for a detailed be illustrated by the fact that the most-visited cook- description). The estimation of vulnerability is based ing website, allrecipes.com, attains about 24 million on the species’ life history (i.e. maximum length, age unique visitors monthly. Online recipes are not only a at first maturity, longevity, von Bertalanffy growth source of public influence but, to a certain extent, parameter K, natural mortality rate and fecundity) could also reflect consumer preferences, since users and ecology (i.e. strength of spatial behavior and can post their own recipes. geographic range). Vulnerability is a metric of Recipes have not been evaluated on a large scale extinction risk and ranges from 0 (lowest) to 100 from a sustainability point of view. Testing the rela- (highest). Mean landings per taxon for 1990 to 2007 tion between the prevalence of different fish taxa in were estimated from the landings reported by recipes and their availability (landings) and vulnera- Moutopoulos & Stergiou (2012). All scientific names bility can reveal whether recipes could act as a driver were obtained from FishBase (Froese & Pauly 2012). for unsustainable use of marine resources. In addi- The relation between recipe prevalence, landings tion, the form of the relation could provide directions and vulnerability was described using stepwise for the conservation of fish stocks. Here, we tested multiple regression, and the reported p-values are this relation using the marine fish taxa in all online 2-tailed. Greek recipes.

RESULTS MATERIALS AND METHODS Of the 3858 recipes found, 179 (4.6%) referred to We analyzed the prevalence of different fish taxa fish without specifying a taxon and thus were in Greek recipes and related the number of recipes in excluded from our analysis. In the remaining 3679 which each taxon appears (henceforth called recipe recipes, there were 4265 occurrences of identified prevalence) with the taxon’s landings and intrinsic taxa (i.e. 1.1 fish per recipe, as some recipes sug- vulnerability to fishing. We examined all online gested >1 taxon) corresponding to 80 Greek common recipes that were available on every website listed in names, 2 of which (perch and tilapia) could not be the catalogs of 2 Greek cooking recipe search assigned to a specific taxon. This is because these 2 engines (www.sintagoulis.gr and www.cookle.gr, taxa, both derived from aquaculture, are sold without accessed December 2011). any information on scientific names. The remaining Overall, we collected 3858 recipes using fish as a 78 common names were assigned to 71 taxa, of which primary or secondary ingredient. These recipes were 60 (84.5%) were at the species level, 8 (11.3%) at the derived from 129 websites, covering a wide variety of genus level and 3 (4.2%) at the family level (Table sources (i.e. recipe web sites, cooking blogs, news - A1). Overall, 15 taxa (20.55%) accounted for 3234 papers, online magazines and television cooking pro- (75.8%) of the occurrences (Fig. 1). grams). In the vast majority of cases, no information was provided regarding the date of recipes or whether recipes posted on the web were actually taken from other sources (e.g. from a published recipe book). All fish common names were assigned to the lowest possible taxon. European hake and Gadus morhua have the same Greek common name (‘bakaliaros’). The former is only sold fresh, while the latter is sold as salted fillets or frozen. Thus, ingredients referring to fresh ‘bakaliaros’ were assigned to M. merluc- cius and the remaining ones to G. morhua. Intrinsic vulnerability to fishing, hence- forth called vulnerability, was taken from Fig. 1. Number of recipes (bars) and cumulative percentage (line, right FishBase (www.fishbase.org; Froese & y-axis) by rank for all fish taxa (n = 71) cited as ingredients in Pauly 2012), as estimated by a fuzzy logic Greek online recipes Apostolidis & Stergiou: Recipes and conservation of fish stocks 301

Fig. 2. Distribution of (a) recipe prevalence (number of recipes in which each taxon appears), (b) vulnerability and (c) mean landings for the fish taxa cited in Greek online recipes. x-axis labels denote midpoints of bins

The distributions of recipe prevalence, vulnerabil- ability and mean landings was stronger (R2 = 0.405, p ity and mean landings for the different taxa are < 0.001, df = 2,31, F = 10.529): log(recipe prevalence) shown in Fig. 2. Recipe prevalence ranged from 1 = −3.223 + 0.444 log(mean landings) + 1.940 log(vul- (0.02%) to 595 (14.0%) recipes (Fig. 2a, Table A1), nerability) after excluding 3 apparent outlier taxa with a mean value (±SD) of 58 ± 105.33. Vulnerability (Engraulis encrasicolus, Solea solea and white ranged from 25, for European anchovy Engraulis grouper Epinephelus aeneus) above the regression encrasicolus, to 88, for sturgeon Acipenser sturio and line and 4 taxa (blotched picarel maena, Atlantic halibut Hippoglossus hippoglossus, with a annular seabream Diplodus annularis, blue whiting mean value of 52.8 ± 16.52 and a main mode at 40 to Micro mesistius poutassou and round sardinella Sar- 45 (Fig. 2b). Mean landings (Fig. 2c) ranged from dinella aurita) below the regression line. 84.3 t, for shi drum Umbrina cirrosa, to 17798 t, for European sardine Sardina pilchardus. We confined our analysis to marine wild stocks DISCUSSION native to Greece (57.8% of recipe citations), exclud- ing cultured (25.6%), imported (15.4%) and freshwa- The fact that recipe prevalence increased with ter species (1.2%). The most prevalent of the 55 mar- landings indicates that the regional cooking culture ine taxa cited in 2467 recipes were Engraulis is developed based on the more abundant species in encrasicolus, followed by Thunnus spp. and common the area. Yet, recipe composition applies a greater sole Solea solea, with 286 (11.6%), 284 (11.5%) and 226 (9.2%) occur- rences respectively (Table A1). For the 41 Greek native marine taxa for which landings were avail- able, the following multiple regres- sion was found (R2 = 0.216, p = 0.039, df = 2,38, F = 5.230): log(recipe prevalence) = −2.852 + 0.471 log (mean landings) + 1.645 log(vulner- ability). The 2 predictors were not intercorrelated (n = 41, r = 0.176, p = 0.271). Thus, after correcting for the effect of landings (partial r = 0.409, p = 0.009), recipe prevalence was significantly correlated (partial r = 0.322, n = 41, p = 0.040) with vulner- ability, indicating that more vulner- able species appear more frequently Fig. 3. Plot of recipe prevalence (number of recipes in which each taxon ap- pears), after removing the effect of landings (residual recipe prevalence), versus in recipes (Fig. 3). The relation vulnerability to fishing for 41 Greek native marine fish taxa cited in online between recipe prevalence, vulner- recipes 302 Mar Ecol Prog Ser 465: 299–304, 2012

pressure on more vulnerable fish species as resented in our sample of recipes (compared to that unmasked after correcting for landings. This can be of Levin & Dufault 2010) is clearly attributed to the explained by the fact that fish taxa with very high multispecies nature of the Mediterranean fisheries landings are not proportionally represented in (Stergiou et al. 1997). In areas supporting multi- recipes. However, the direction of causation for the species fisheries, it could be relatively easier to re- above relation is not easy to identify, and in any case, orient the public toward consuming less vulnerable our aim was to highlight the trend and its implica- species. In contrast, in northern areas supporting tions for the conservation of fish stocks. This trend fisheries made up of relatively few species, con- should be changed by decreasing the recipe abun- sumers have fewer options for such a reorientation, dance of taxa that are very vulnerable to fishing and unless they are directed to imported species. The counterbalance such a reduction with an increase in latter, however, might drive imported species to the representation of taxa of low vulnerability, which depletion in their native ecosystems (Pelletier & are landed in large quantities and currently under- Tyedmers 2008). represented in recipes. The interaction between online recipes and con- Various ways exist for reversing the above men- sumer preferences can be masked by various issues. tioned trend. For example, editors of recipe websites For example, many individuals purchase ingredients could ban publication of recipes that have as ingredi- without consulting recipes, and others enjoy reading ents very vulnerable species, and also remove such recipes that they might never prepare or might recipes that are already posted. At the same time, edi- replace certain ingredients with more easily avail- tors in close cooperation with chefs, could promote able or affordable substitutes. In addition, online recipes with less vulnerable species, providing at the recipes might be a biased sample of available same time necessary information (e.g. vulnerability recipes. Yet, there is no doubt that in the digital era, and exploitation patterns) on such environmentally more and more people will rely on online recipes responsible choices. For the Greek online cuisine, in within the ‘internet life style’ framework as is true for particular, recipes with taxa such as dusky grouper e.g. scientific literature, books, newspapers and Epinephelus marginatus and red porgy Pagrus pagrus other consumer goods. This is especially true of (both assessed as endangered by the International recipes for which a quick search online is preferable Union for Conservation of Nature) should be removed for day-to-day cooking. Thus, the influence of recipes and replaced by less vulnerable taxa such as Spicara on consumer consumption is expected to drastically maena, Sardinella aurita, Diplodus annularis and increase in the near future. Micromesistius poutassou (see Fig. 3). The strong enforcement of fisheries management The realization of a change in consumer prefer- measures at various levels is the only certain way to ences through recipes would require first that recipes reduce overfishing (Worm et al. 2009). However, can adjust with time and second the education and since consumer demand for fish will continue to active participation of chefs and recipe authors in increase, and fisheries management cannot always order to exploit their skills to strongly influence con- be effective, alternative management actions may sumers. Levin & Dufault (2010), by analyzing seafood also be necessary. Managing aspects of culture that recipes published in cookbooks from 1885 to 2007, strongly influence the public, such as recipes, by showed that the mean trophic level of seafood repre- educating a small group of stakeholders (i.e. chefs sented in recipes increased with time (eating up the and recipe authors) may be a cost-effective way of food web). This finding shows that recipe composi- promoting fisheries sustainability. tion can change with time. Suggestions made by cul- tural icons in the cooking industry (e.g. television Acknowledgements. The authors thank E. Schultz, A. Tsikli- cooking show presenters) can influence and shape ras, D. Moutopoulos and 3 anonymous reviewers for critical consumer preferences, possibly much more than sci- comments and suggestions. entists and other stakeholders can. A good example is the late celebrity chef Julia Child, who promoted LITERATURE CITED consumption of American angler Lophius ameri- canus in the USA through her popular television Cheung WWL, Pitcher TJ, Pauly D (2005) A fuzzy logic cooking show (Weber 2002). expert system to estimate intrinsic extinction vulnerabil- ities of marine fishes to fishing. Biol Conserv 124:97−111 Consumer preferences are presumably more mal- Failler P, Pan H (2007) Global value, full value and societal leable when the marketplace has a diversity of costs: capturing the true cost of destroying marine eco- choices. The large number of native fish species rep- systems. Soc Sci Inf (Paris) 46: 109−134 Apostolidis & Stergiou: Recipes and conservation of fish stocks 303

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Appendix 1

Table A1. Assigned taxon, Greek and English common names, number (N) of recipes citing the taxon, vulnerability index (Vuln.) and mean landings (±SE; in t), for all fish cited in online Greek recipes. The vulnerability to fishing index (see text for definition) ranges from 0 to 100, with 100 representing the taxon most vulnerable to fishing. na: not available

Taxon Greek name English name N Vuln. Landings (t)

Native marine Engraulis encrasicolus Gavros European anchovy 286 25.0 13 820.1 ± 550.7 Thunnus spp. Tonoi Tuna 284 70.0 3075.3 ± 202.7 Solea solea Glossa Common sole 226 41.0 1852.7 ± 136.4 Sardina pilchardus Sardela European pilchard 204 36.0 17 798.6 ± 953.5 Epinephelus aeneus Sphyrida White grouper 161 52.0 154.62 ± 7.3 Xiphias gladius Xiphias Swordfish 111 72.0 2937.15 ± 91.9 Dentex dentex Sinagrida Common dentex 106 67.0 589.41 ± 16.6 Mullus surmuletus Barbouni Surmullet 105 36.0 2673.52 ± 127.8 Merluccius merluccius Bakaliaros freskos European hake 87 71.0 7354.3 ± 218.7 Epinephelus marginatus Rofos Dusky grouper 84 72.0 190.5 ± 9.0 Lophius spp. Peskandritses Monkfish 82 70.5 2129.6 ± 103.8 Pagrus pagrus Phagri Red porgy 73 66.0 744.8 ± 16.8 Triakidae Galeos/glaukos Houndsharks 64 61.5 1139.9 ± 50.3 Scorpaena spp. Skorpioi Scorpionfishes 63 53.0 1472.8 ± 55.1 Scomber colias Kolios Atlantic chub mackerel 57 46.0 4960.4 ± 772.4 Pagellus erythrinus Lithrini Common pandora 54 54.0 2286.0 ± 78.0 Marida Picarel 41 39.0 5072.4 ± 551.5 Boops boops Gopa Bogue 35 45.0 7475.1 ± 721.9 Sarda sarda Palamida Atlantic bonito 32 33.0 2350.3 ± 97.1 Scomber scombrus Skoumbri Atlantic mackerel 30 44.0 912.3 ± 203.0 Mugilidae Kefalos Mullets 26 47.4 6468.7 ± 185.0 Atherina boyeri Atherina Big-scale sand smelt 22 43.0 na Mullus barbatus Koutsomoura Red mullet 17 42.0 3735.1 ± 95.9 Seriola dumerili Magiatiko Greater amberjack 17 54.0 675.5 ± 40.8 Diplodus sargus Sargos White seabream 17 63.0 1386.5 ± 38.2 304 Mar Ecol Prog Ser 465: 299–304, 2012

Table A1 (continued)

Taxon Greek name English name N Vuln. Landings (t)

Serranus spp. Mpoukanares/chanoi/perkes Combers 17 44.3 365.6 ± 29.8 Zeus faber Christopsaro John dory 16 39.0 283.8 ± 22.7 Triglidae Kaponia/chelidonopsara Gurnards 13 38.3 259.0 ± 24.6 Trachurus spp. Savridia Jack mackerels 13 45.7 6967.1 ± 723.3 Sarpa salpa Salpa Salema 12 41.0 583.2 ± 47.0 Raja spp. Vatoi/Rines Rays 11 58.7 1013.8 ± 47.8 Sparisoma cretense Skaros Parrotfish 9 36.0 na Polyprion americanus Vlachos Wreckfish 9 72.0 506.3 ± 16.3 Umbrina cirrosa Milokopi Shi drum 8 40.0 84.3 ± 5.9 Pomatomus saltatrix Gofari Bluefish 7 59.0 692.8 ± 34.9 Lithognathus mormyrus Mourmoura Sand steenbras 7 40.0 na Epinephelus costae Stira Goldblotch grouper 6 66.0 na Belone belone Zargana Garfish 6 39.0 238.8 ± 26.7 Trachinus draco Drakaina Greater weever 5 42.0 na Uranoscopus scaber Lichnos Stargazer 5 32.0 na Sphyraena sphyraena Loutsos European barracuda 5 75.0 na Tseroula/menoula Blotched picarel 5 33.0 6166.8 ± 581.2 Oblada melanura Melanouri Saddled seabream 4 34.0 765.0 ± 87.1 Conger conger Mougri European conger 4 86.0 1067.8 ± 96.3 Labrus spp. Chiloudes/petrochiloudes Wrasses 3 39.0 na Xyrichthys novacula Rouzeti Pearly razorfish 3 36.0 na Muraena helena Smerna Mediterranean moray 3 74.0 na Scophthalmus maximus Kalkani Turbot 3 51.0 127.7 ± 7.2 Coryphaena hippurus Kinigos Common dolphinfish 2 39.0 na Mycteroperca rubra Piga Mottled grouper 2 81.0 na Pagellus acarne Mousmouli Axillary seabream 1 43.0 na Phycis spp. Salouvardos Forkbeards 1 54.5 na Diplodus annularis Sparos Annular seabream 1 35.0 786.56 ± 52.6 Micromesistius poutassou Prosfigaki Blue whiting 1 33.0 1284.0 ± 116.2 Sardinella aurita Frisa Round sardinella 1 36.0 1558.5 ± 220.1 Native freshwater Cyprinus carpio Grivadi Common carp 23 65.0 na Anguilla anguilla Xeli European eel 21 70.0 na Esox lucius Tournas Northern pike 3 69.0 na Rutilus rutilus Tsironi Roach 2 37.0 na Silurus glanis Goulianos Wels catfish 1 87.0 na Acipenser sturio Mourouna Sturgeon 1 88.0 na Imported Gadus morhua Bakaliaros kseros (gados) 595 65.0 na Beryx decadactylus Kokkinopsaro Alfonsino 32 72.0 na Clupea harengus Rega Atlantic herring 24 36.0 na Hippoglossus hippoglossus Ippoglosos Atlantic halibut 3 88.0 na microlepidota Black cod Black cod 1 62.0 na Aquacultured Salmo salar Solomos Atlantic salmon 502 na na Not specified Perka Perch 175 na na Sparus aurata Tsipoura Gilthead seabream 166 na na Dicentrarchus labrax Lauraki European seabass 139 na na Oncorhynchus mykiss Pestrofa Rainbow trout 87 na na Pangasianodon Pagasios Striped catfish 19 na na hypophthalmus Not specified Tilapia Tilapia 4 na na

Editorial responsibility: Christine Paetzold, Submitted: March 14, 2012; Accepted: June 22, 2012 Oldendorf/Luhe, Germany Proofs received from author(s): September 19, 2012